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203 Insulin Gene Therapy of Diabetes in Mice by Glucose Regulated Helper Dependent Adenoviral Vectors Molecular Therapy �������� ��� ���� ���������������� �������� ���� ������© ����������� �!����� ���[.]

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Molecular Therapy Vol 7, No 5, May 2003, Part 2 of 2 Parts

levels decreased to the normal range within 2 weeks after treatment

and normal levels were maintained for at least 4 months, whereas

untreated diabetic ob/ob mice remained hyperglycemic We examined

the presence of the LPK-MI genome in various tissues by PCR at

one month after treatment with rAAV-LPK-MI We detected the

LPK-MI genome in all tested tissues including the liver, kidney,

spleen, lung, and heart, with the highest amounts in the liver and

spleen When we examined the expression of MI mRNA in various

tissues by reverse transcriptase-PCR, we found that MI mRNA

was expressed mainly in the liver, suggesting that the expression of

MI mRNA is dependent on the liver-specific L-type pyruvate kinase

promoter activity To determine whether rAAV-LPK-MI-treated

ob/ob mice clear glucose from the blood, we performed glucose

tolerance tests at 6 weeks after rAAV-LPK-MI administration We

found that the glucose level peaked at 30 min after glucose injection

and returned to normal within 180 min, whereas the blood glucose

levels of untreated diabetic ob/ob mice were not normalized In

addition, we performed insulin tolerance tests to determine the effect

of rAAV-LPK-MI treatment on insulin resistance Although insulin

resistance in rAAV-LPK-MI-treated ob/ob mice was significantly

alleviated compared to untreated diabetic ob/ob mice, some insulin

resistance was still present as compared to heterozygous ob (+/-)

mice These results suggest that this insulin gene therapy may have

potential therapeutic value for the treatment of obese type 2 diabetes

Peptide 1 for Gene Therapy of Type 2 Diabetes

Donna Armentano,1 Geoffrey Parsons,1 David Souza,1 Dan Yu,1

Samuel Wadsworth,1 Richard Gregory.1

1 Genzyme Corporation, Framingham, MA, United States.

Glucagon-like peptide 1 (GLP-1) is an incretin hormone produced

in the gut in response to nutrient intake and acts in several ways to

reduce post-prandial blood glucose excursions It is a potent

stimulator of glucose-induced insulin secretion, delays gastric

emptying, suppresses glucagon secretion, improves insulin

sensitivity in peripheral tissues and more recently has been shown

insulinoptropic actions of GLP-1 have made it a promising candidate

for the treatment of type 2 diabetes However, the short in vivo

half-life of GLP-1, due to inactivation by dipeptidylpeptidase IV

(DPPIV), has made protein-based treatments challenging requiring

repeat subcutaneous injections or continuous infusion of peptide

A gene therapy approach using vectors to express a DPPIV resistant

analog is one way to circumvent the rapid turnover of GLP-1 and

need for repeat administration We have developed GLP-1 chimeric

expression vectors encoding a DDPIV-resistant 31-amino acid

peptide linked to leader sequences required for secretion of GLP-1

Plasmid or adenoviral expression vectors were administered via tail

vein to diabetic db/db mice in both the C57BL/KsJ (more severe

diabetes) and C57BL/6 (less severe diabetes) genetic backgrounds

Plasma GLP-1, blood glucose, insulin, body weight and %HbA1c

were monitored over time Constitutive secretion of GLP-1 in vivo

resulted in plasma levels of GLP-1 >1nM which were sustained for

periods longer than 1 month Expression of GLP-1 led to lowering

either fasting or random fed hyperglycemia, and consequently,

%HbA1c in these mice These results demonstrate proof-of-concept

for GLP-1 gene therapy of type 2 diabetes using GLP-1 expression

vectors and provide a means for circumventing the need for

continuous infusion of GLP-1 or subcutaneous injection

Liver by Systemic Administration of a Recombinant Adenovirus Expressing a Furin-Cleavable Mouse Preproinsulin Can Remit Diabetes in Diabetic NOD Mice and Evade Autoimmune Attack

Seungjin Shin,1 Jaeseok Han,1 Hee-Sook Jun,1 Ji-Won Yoon.1

1 Julia McFarlane Diabetes Research Centre, The University of Calgary, Calgary, AB, Canada.

Type 1 diabetes results from the destruction of pancreatic beta cells caused by autoimmune-mediated immune responses Restoration of beta cells by islet transplantation or regeneration of pancreatic beta cells from ductal stem cells are attractive methods for the cure of diabetes; however, it is difficult to overcome the hostile beta cell-specific autoimmune responses that might eventually destroy the transplanted or regenerated beta cells Since the liver is

an attractive target for insulin gene therapy, this investigation was initiated to determine whether transduced, insulin-producing hepatocytes can evade autoimmune attack and remit hyperglycemia

in the nonobese diabetic (NOD) mouse, which spontaneously develops autoimmune diabetes We constructed a recombinant adenovirus expressing a furin-cleavable mouse preproinsulin under the cytomegalovirus promoter and the beta-globin/IgG chimeric intron, which will constitutively express insulin (rAd-CMV-mPPI)

In vitro studies showed that an immortalized hepatocyte cell line transduced with rAd-CMV-mPPI produced biologically active insulin

To test this gene construct in vivo, we administered rAd-CMV-mPPI (5 × 109 particles) intravenously through the tail vein of spontaneously diabetic NOD mice (blood glucose > 400 mg/dl) and found that blood glucose was reduced to normal levels within 2 days after administration and maintained at normoglycemic levels for one month, after which time the experiment was terminated We examined the expression of insulin in various tissues, including the liver, kidney, spleen, stomach, heart, pancreas, and lung, and found that insulin was mainly expressed in the liver, as compared to other organs, suggesting that systemic administration of rAd-CMV-mPPI resulted

in delivery mainly to liver tissue To determine whether these insulin-producing hepatocytes are attacked by existing effector T cells in the recipients, we examined the liver at 7, 14, 21, and 30 days after rAd-CMV-mPPI administration We found that the liver was not invaded by effector cells such as T cells and macrophages When we adoptively transferred splenic lymphocytes from the rAd-CMV-mPPI-treated NOD mice into NOD.scid mice, over 90% of the recipients developed diabetes within 7 weeks, indicating that effector cells in the rAd-CMV-mPPI-treated NOD mice were active Based

on these observations, we conclude that constitutive expression of insulin in the liver by systemic administration of rAd-CMV-mPPI can remit diabetes and evade autoimmune attack in diabetic NOD mice

by Glucose-Regulated Helper-Dependent Adenoviral Vectors

Paola Corbella,1 Laura Perani,1 Francesca Mingozzi,1 Alessandra Recchia,1 Fulvio Mavilio,3 Maria-Grazia Roncarolo,1 Luca Falqui.1,2

1 San Raffaele-Telethon Institute for Gene Therapy, San Raffaele Hospital Scientific Institute, Milan, Italy; 2 Medicine,

Endocrinology and Diabetes Unit, San Raffaele Hospital Scientific Institute, Milan, Italy; 3 Department of Biomedical Science, University of Modena School of Medicine, Modena, Italy.

Type 1 diabetes is an autoimmune disease characterized by destruction of insulin-producing pancreatic beta cells, resulting in

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Molecular Therapy Vol 7, No 5, May 2003, Part 2 of 2 Parts

Copyright © The American Society of Gene Therapy

S80

deficient insulin secretion and hyperglycemia Despite intensive

insulin therapy, properly controlled glucose values are hardly

achieved, therefore degenerative chronic complications may arise

In search for alternative therapeutic options, this project aims at

engineering non-beta cells for the production of insulin in a

glucose-regulated manner The liver is the candidate target organ for this

purpose, as hepatocytes are able to ‘sense’ extracellular glucose

variations and modulate consequentially gene expression To obtain

efficient insulin expression in the liver, we are exploring

Helper-Dependent Adenoviral Vectors (HD-AdV), which should also

provide a better safety profile We generated a vector coding for

Furine cleavable-Human Proinsulin (FurHPI) under the control of

the glucose-responsive liver-specific Pyruvate Kinase gene promoter

(L-PKp) coupled to the SV40 enhancer The vector was injected

into STZ-induced diabetic immunodeficient’nude’ mice (n=4/group)

at two different doses: 1.4x10e11 (low dose) or 2,8x10e11 (high

dose) vp/mouse Human insulin was detectable as early as the first

week after virus injection in both groups, reaching a maximum

group and of 129-192 μU/ml in the high-dose group, and remaining

at similar levels thereafter Mice injected with the low dose remained

hyperglycemic whereas with the high dose blood glucose returned

to normal value, starting from the 2nd week At 4 weeks, the high

dose produced exceedingly high insulin levels (normal insulin values

level was reduced to moderate-severe hypoglycemic value (53±8

mg/dl) Glucose loads and fasting tests demonstrated that L-PKp

displays a slow and weak (3.6-fold over 4 h) induction and 6-fold

repression of insulin synthesis upon glucose increase/decrease We

then generated a second vector containing a Hybrid(L-PK/Spot14)

promoter, which displayed a stronger response to glucose than the

L-PKp once transfected in rat hepatocytes We linked this promoter

to the nuclear LacZ reporter gene in order to quantify liver expression

and tissue specificity This vector was injected into ‘nude’ mice

(n=2) at the dose of 2,8x10e11 particles/mouse Animals were

sacrificed and tissues collected 4 weeks post-gene transfer and

activity was detected in liver extracts only, indicating that this

promoter maintains liver-restricted expression Hepatocytes toxicity

was determined by liver enzyme function test AST and ALT peaked

(x5) at day 1 after injection, then returned to normal level at day 7

The reporter gene will be replaced with FurHPI to obtain faster

glucose-responsive induction of insulin synthesis in liver cells These

results indicate that HD-AdVv are suitable vectors to pursue a

fine-tuned glucose-responsive insulin expression in the liver for gene

therapy of type 1 diabetes

Interleukin-10 (IL-Interleukin-10) for Prevention of Type 1 Diabetes in

NOD Mice: Comparison of Mutant (I87A

Substitution) to Recombinant Murine IL-10

Matthias H Kapturczak,1 Clive H Wasserfall,2 Scott Loiler,3

Cross,2 James M Crawford,2 Tamir M Ellis,2 Terence Flotte,3

1 Medicine, University of Florida, Gainesville, FL; 2 Pathology,

Immunology and Laboratory Medicine, University of Florida,

Gainesville, FL; 3 Pediatrics, University of Florida, Gainesville,

FL.

Type 1 diabetes results from the autoimmne destruction of the

underlying this process are unclear, immunoregulatory defects appear

to be associated with genetic susceptibility and disease progression

Previous studies have demonstrated that a single intramuscular (I.M)

injection of recombinant adeno-associated virus (rAAV) vector (serotype 1) containing the murine IL-10 gene, in a dose and time-dependent fashion, consistently and dependably prevents type 1 diabetes and insulitis development in female non-obese diabetic (NOD) mice However, histological evaluation of the muscle injection sites receiving rAAV-IL-10 revealed long term evidence of myositis and atrophic muscular changes Additional studies have suggested that a substitution of isoleucine at position 87 of IL-10 with alanine inhibits some of the immunostimulatory functions of IL-10, rendering the mutated molecule a potentially more safe agent for studies aimed

at disease prevention To compare IL-10 with I87A-IL10 in terms

of diabetes prevention and side effect profiles, groups of 4 week-old female NOD mice (n=13 animals per group) were I.M injected with

109 infectious units (IU) of rAAV-IL-10, 109 IU of

(encoding the first 33 amino acids of IL-10 and not biologically active) and saline as controls Urine glucose levels were monitored weekly for disease development, with disease rates assessed by life-table (Kaplan-Meier) analysis At 14 weeks post injection, 3 animals from each group were sacrificed for histological and immunological assesments At 38 weeks post injection, diabetes frequency was as follows: IL-10 0% p=0.0016 vs saline, 0.0671 vs delta-IL-10), 109 IU I87A 20% NS vs controls), 107 IU I87A 60%, delta-IL-10 30% and saline 50% In terms of the prevention of insulitis, the degree of infiltration essentially mirrored that of diabetes development with high-dose IL-10 proving most effective.Unlike the saline and delta-IL-10 groups, the IL-10 group and both I87A-IL-10 groups showed development of significant infiltrate of the muscle at the injection site Phenotyic analysis (CD3, CD4, CD8, macrophage, B-lymphocyte) revealed this inflitrate to be predominantly B-lymphocyte in origin Significant muscle fiber atrophy, however, was seen only in the IL-10 group Our study demonstrates that I87A-IL-10, was less efficient than IL-10 in terms

of diabetes prevention Furthermore, such substitution did not abrogate the chemotactic properties of IL-10 Studies of other mutations in the IL-10 structure will be necessary to select for only the desirable parts of the IL-10 function repertoire; allowing for effective disease prevention and devoid of sequence allowing for potentially deleterious inflammation

for the Treatment of Lysosomal Storage Disease

in the Brains of MPS I Mice

Gordon Watson,1 Jacob Bastacky,1 Steve Jungles,2 Michael Vellard,2 Pavel Belichenko,3 Emil Kakkis.2

1 Children’s Hospital Oakland Research Institute, Oakland, CA;

2 BioMarin Pharmaceutical, Novato, CA; 3 Stanford University, Stanford, CA.

Mucopolysaccharidosis Type I (MPS I) is caused by an inherited deficiency of α-l-iduronidase (IDU) The result is a progressive, lysosomal storage disease that includes CNS as well as systemic involvement Enzyme replacement therapy by periodic intravenous infusion of purified IDU has been shown to be effective in treating the non-CNS manifestations of the disease; however, the blood brain barrier excludes therapeutic levels of IDU in the brain Thus, our goal was to develop gene therapy for MPS I specifically targeting the brain Although the blood brain barrier also excludes viral vectors that are administered intravenously, initial studies with a similar storage disease, MPS VII, indicated that intrathecal administration

of an AAV vector could circumvent this problem For MPS VII experiments, which eliminated storage vacuoles throughout the brain,

a relatively high dose of 5 x 1011 vector particles per adult mouse was used To treat MPS I mice, AAV-IDU vectors with and without the woodchuck hepatitis virus posttranslational regulatory element (WPRE) were constructed These vectors contained human IDU

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